And Taxonomy

Page 165 BACTERIOLOGICAL NOMENCLATURE AND TAXONOMY

THE YEASTS= A TAXONOMIC STUDY A Review R. E. Buchanan, Ames, Iowa, U.S.A.

This volume of 713 pages by Dr. J. Lodder, mycologist of Koninklijke Nederlandsche Gist- en Spiritusfabriek of Delft and Dr. N. J. W. Kreger van Rij, mycologist of the Cen- traalbureau voor Schimmelcultures, Yeast Division, Delft, is a highly welcome and authoritative summary of our know- ledge of the yeasts. It may be regarded as a revision and condensation of the several volumes on taxonomy and nomenclature of the yeasts previously prepared by the staffs at Baarn and at Delft.

The introductionnotes that specific epithets previously given to yeast species by earlier authors have in general been corrected in this text when not formed in conformity to the articles and recommendations of the revised International Botanical Rules of Nomenclature.

After a survey of literature and experience, the authors, for purposes of genera and species differentiation, fix upon six morphological character8 (characteristics of vegetative re- production, shape and size of cells, ascospore formation, ballistospores, and colony characteristics)and twelve physiological properties (pellicle formation, fermentation, sugar assimilation, utilization of nitrate, utilization of ethanol as a sole source of carbon, splitting of arbutin, production of carotenoid pigments, production of starch-like compounds , production of esters, reaction in litmus milk, splitting of fat, and acid production). These are clearly defined and the methods for laboratory determination outlined.

The taxonomic problems related to yeast variability are reviewed with understanding and discrimination. The artifi - cia1 nature of the group called yeasts is satisfactorily em- phasiaed, as well as the practical utility of this grouping.

Three families are recognized, the E n d o my c e t a c e a e including yeasts which form asci and ascospores, the S Q o r o b o 1 o m y c e t a c e a e which produce so-called ballistospores on sterigmata fromwhich they are forcibly dis- Page 166 INTERNATIONAL BULLETIN charged, (resembling the spores of the Basidiomyce - -t e s ), and the asporogenous yeaets placed in the C r ypt o - c occaceae.

The ascogenous yeasts are included in the fungus class Ascomycetes, the subclass Protascales andthe order Endomycetales. Asingle ascogenous yeast family is recognized, the Endomycetaceae which in turn includes five subfamilies, as follows: Eremascoideae, with one genus Eremascus E nd o my c e toi de a e , with two genera, E nd omyc e s and S c hi z o s a c c ha r o myc e s . S a c c ha r omy c e t oide a e , with three tribes Endomycopseae, with one genus Endomycop- -sis -Sac char omyce te ae ,withfive genera, S acc har o- myces, Pichia, Hansenula, Schwann- iomyces and Debaryomyces. Nadsonieae, with three genera, Saccharomy- codes, Hanseniaspora and Nadsonia. Nematosporoideae, with three genera, Monospo- rella, Nematospora, and Coccidiascus. Lipomycetoideae, with one genus, Lipomyces.

There are several anomalies in the above nomenclature that deserve comment. On the basis of the directives of the Bo- tanical Code, the name of the family Endomycetaceae is derived from the name of the containedgenus, E n do my - c e s . The inappropriateness of the family name is evident from the footnote (p. 53) which states:-. "This genus does not belong to the yeasts in the proper sense". The authors do not discuss in detail the priorities of the names Endo- mycetales and Saccharomycetales for the order, nor of Endomycetaceae and Sac char omycetaceae for the family. This failure on the part of the authors to justify the use of names of taxa higher than the genus is un - fortunate. The recognition of Endomycetaceae as the family name is apparently based upon the statement of Stel- ling-Dekker (1931, p. 522) who says:-

"Unter diesen Umsthden empfiehlt es sich,die in dieser Abhandlung beschriebenen Organismen - also neben den Page 167 BACTERIOLOGICAL NOMENCLATURE AND TAXONOMY

typischen Hefearten auch die Vertreter der Gattung En- d o myc e s - in einer Familie woftir dann der altere =- men Endomycetaceae angebracht ist, vereinigt zu halten.

A hasty examination of the literature seems to indicate that the Stelling-Dekker statement may be incorrect. The first definite use of Saccharomycetaceae asafamily name found by the writer is that of DeToni (1889, p. 916) in Saccar- do's Sylloge Fungorum. He ascribes the name to Reess (1870). A study of the paper by Reess fails to confirm such use of the name; the family name was not given by Reess. The first use of the name Endomycetaceae found is that of Schroeter (1897 p.154) in the Pflanzenfamilien of Engler and Prantl. If all of the yeast genera are to be included in a single family, it would seem that the family name should be Saccharomycetaceae.

It is of interest tonote that the authors list three species of Endomyces, describe none of them, and in effect, re- move them from consideration as yeasts.

The writer believes that nomenclatural confusion and taxonomic difficulties will be minimized if the older differenti- ationof the two families, Saccharomycetaceae and E n d o m y c e t a c e a e is maintained. The apparent nom - enclatural centering of the whole group of yeasts around an ascus-bearing mold (E n domy c e s d e c i p i e n s ) parasi- tic upon the gills of a single species of mushroom makes for confusion.

Beginning with the description of the genus Sc hiz o s a c - charomyc e s (p. 81) the format is a model for microbio- logical systematic monographs. The fifteen genera of the E n d o m y c e t a c e a e are differentiated in a well-organiz- ed dichotomous key. For each genus there is included a genericdiagnosis, the designation of the type species of the genus, an historical survey of the generic name, a list of the species recognized, and a dichotomous key to the species. This is followed by a systematic discussion of each species, including synonyms, original description and historical survey, standard description ( morphological and Page 168 INTERNATIONAL BULLETIN

physiological characters ), origin and char acte rization of strains studied and designation of the type strain of the species. Drawings of the vegetative and sporulating cells are generally included.

One may question the author's ascription for some of the genera, as for example, (p. 116) the genus S a c c ha r om y - -ces (Meyen) Reess. It would seem that this should be S a c c ha r omy c e s Meyen, for this author named both the genus and the type species. Possibly the authors intended Saccharomyces Meyen emend, Reess.

Inasmuch as the type species must be one of those included in the first publication of the genus, the type should probably be designatedSaccharomyces cerevisiae Mey- en emend. Hansen. In several other cases the name of the emending author has been substituted for the name of the original proponent of the name.

The following comments as to other unresolved nomenclatural problems may be made.

1. Clements and Shear (1931 p. 246) apparently designated Saccharomycopsis capsularis Schi6nning as the type species of the genus Saccharomycopsis. Lod- der and van Rij (1952) designate S. guttulata as the type species and recognize the trGfeqcap - sularis to the new genus Endomycopsis Dekker {- {- designate (1952) this as the type species of the genus Endomycopsis. A careful review should be made to determine whether by virtue of the designation of the same type species for each of the two genera, the genus E n domy c op s i s is not in fact a later synonym of Saccharomycopsis, It would appear that Sac- charomycopsis guttulata is the type species of a nameless genus.

2. On page 96, and on later pages, the recognized species of each genus are listed "in chronological sequence", that .is, in the order in which they were described. The format used is one that may give rise to a misinterpre - tation. The name ttEndomycopeis capsularis Page 169 BACTERIOLOGICAL NOMENCLATURE AND TAXONOMY

(Schihning) Dekker 1913" would usually be interpreted as meaning that Dekker placed the organism in the genus Endomycopsis in1913, andnot that Schionning originally described it in that year.

3. The type species of Saccharomyces was designated as -S . c e r e v i s i a e by Clements and Shear (1931 p. 246). 4. (p. 122) Should not the type species have been listed as Saccharomyces cerevisiae Meyen emend. Han- sen ?

5. Reess (not Hansen) named Saccharomyces ellip- soideus, as also -S. exiguus and -S. pas toria- -nus. 6. The genus Deb a r y omyc e s was founded by Klocker upon a single species D. g 1o b o s u s . This would nor - mally, therefore, beregarded as the type species. How- ever, the authors place this first named species in the genus Sacc ha r omyc e s , and as type species designate D e b a r yomy c e s h ans e nii (S acc ha r o my- -ces hansenii Zopf 1889). They further recommend that the emended genus be made a nomen genericum conservandum. This recommendation is made to avoid the necessity of erecting a new name to replace Deb a r y o - myc e s . Careful consideration should be given to the question of the conservation of the name, such action may raise more problems than it will settle. The mat- ter is somewhat further complicated by the fact that Cle- ments inferentially fixed the type species in his designation of Isomyces globosus (Kl6cker)Clements as the type of the genus I s om y c e s proposed as a replace- ment for Debaryomyces.

7. The authors state that Derx (1948) designated S p or ob o - lomyces roseus Kluyver and van Niel as the type species of the genus. This ignores the earlier (1931) designation of 5 s a 1m o ni c o 1o r Kluyver and van Niel as the type species.

8. The authors accept Bulle r a a1b a (Hanna) Derx as Page 170 INTERNATIONAL BULLETIN

designated by Derx (1948) as the type species of Bulle - r a rather than the B u 11 e r a gr a n d i s p o r a proposed 6 Clements and Shear (1931).

9. The Ilasporogenous'l yeasts are placed in the Fungi Impe r f e c ti, with the establishment of a new order, the C r y p t o c o c c a 1e s containing the single family C r yp t o c o c c a c e a e . Unfortunately there is not given adequate consideration of historical background and reasons. No synonymy is given for the names of these higher taxa. Some careful nomenclatural study seems called for.

10. The frank recognition of the generic status of C r yp t o - COC cus is helpful, it may assist in clearing up some of the problems in medical mycology. However, the authors have somewhat oversimplified the problem of such recognition. The type species of C r yp t o c o c c us was designated by Clements andshear (1931) as C r y p t o c o c - cus fermentum Kuetzing. But the only species de- 7 scribed in the original publication by Kuetzing is C. m o 11 i s which would be presumed to be the type rathG than the later C . f e r me nt um . The designation by the authors of Cryptoc oc c us ne of o r man s (Sanfe- 1ice)Vuillemin haa much to commend it, without serious question it would bring some much needed stability. But it would seem that for this typification to be accepted some international sanction is needed. Perhaps the sim- plest, thoughnot the only method of achieving the desired goal, wouldbeforthe authors to recommend to the Inter- national Committee on the Nomenclature of the Fungi that C r y p t o c o c c u s Kuetzing be placed in the list of nomina generica rejicienda and that the generic name C r yp toc o c c u s Vuillemin be recognized as a nomen genericum conservandum with the type species the C r yp t o c oc c u s ne of ormans (Sanfelice) Vuillemin as several times proposed in the literature. Some study also needs to be given to the alternative name -C. hominis.

11. The legitimacy of the name Torulopsis Berlese, as used by the authors, is questioned by themselves. The Page 171 B AC T E R 1'0L 0 G IC A L N 0 ME NC LAT U R E AND TAXONOMY

implications of discarding T o r u 1o p s i s r o s e a as the typeand of replacing it by Torulopsis colliculosa (Hartmann) Saccardo should be carefully reviewed, and any desirable international action recommended,

12. The status of C andida as a generic name is indicated as problematical and tentative. One may hope for a prompt decision from the Committee on the Nomencla- ture of the Fungi appointed by the Stockholm .Botanical Congress, to which Committee the problem has been re- ferred.

13.The type species is designated as Candida albicans (Robin) Berkhout. However, C. vul a r i s Berkhout was chosen by Clements and Shea*he authors note that C. vulgaris Berkhout is to be regarded as a synonpTf C. tr opicalis (Castellani) Berkhout. Should C . tropic ali s be regarded, therefore, as the type specfes?

14. The great amount of work done by the various groups of yeast specialists in bringing order out of zymological chaos is illustrated by the listing of ninety-one synonyms for the species Candida albicans.

15. An interesting complication arises in the discussion of Gandida mycoderma by the authors. The statement is made (p.483):~'Pic hi a me mb r anif a c i e n s Hansen has to be regarded as the perfect stage of this species". The implications of this assertion require careful exploration in thelight of Article 57 of the Inter- national Rules of Botanical Nomenclature, which seems to indicate that the name of the perfect form should be used when known.

16. The reasons for the designation of T r i c h o s p o r o n cu- taneum as the typespeciesof the genus Trichospo- -r on are not sufficiently documented. Behrend (1890) is stated to have "created the genus T r i c h o s p o r on with the single species T. ovoide 8. This species would therefore seem to be the type; however, the authors state Itaccording to Article 18 of the International Page 172 INTERNATIONAL BULLETIN

Rules of Botany Nomenclature T r i c h o s p o r on c u t a - neum (de Beurmann, Gougerot et Vaucher) Ota is the type species of the genus". The writer can find nothing in Article 18 to justify this conclusion. The authors (p. 641) regard T. ov oi de s Behrend as a --nomen du- -bium and rejectx. This reasoning would seem to make the generic name T r i c h o s p o r o n Behrend question- able. Might T . o vo ide s Behrend be identified with one of the more recentlydescribed species, thus making the later description an emendation of that of Behrend? Or the generic name T r i c ho s p o r on Behrend might be rejected and replaced by some later synonym. The authors are probably right in concluding that the accept- ation of T . c u t ane urn as the type species would cause the least confusion in nomenclature. If this is done a suitable request for internation.al approval should be for- mu1at e d.

17. In this reyiew Clements and Shear are several times quo- ted as having designated the type species in certain fungus genera. It should be noted that these authors defin- itely stated that they were designating the types in accor- dance with the well recognized rules of botanical nomenclature, but that the validity of their designations in many cases has been called into question as by Seaver (1932). The fact of these designations must be recognized by later workers, but their legitimacy may require careful checking, A ruling by the appropriate Commit- tee on the legitimacy of the many designations thus made would be of material mycological assistance.

The Latin diagnoses required under the Botanical Code to make legitimate the names of new taxa are given as follows: S a c c ha r o myc e s four species (pp. 668-669). Lipo my c e s genus and one species (p. 669). Cryptococcus one variety (p.670). T o r u 1 o p s i s six species and one variety (pp. 670-671). Candida three species and two varieties (p. 672). Trichosporon one species (p.673). Page 173 BACTERIOLOGICAL NOMENCLATURE AND TAXONOMY

The author and taxonomic indices are adequate and admira- ble.

In the opinion of the writer, the time has come when a ser- ies of well formulated recommendations relative to the un- settled nomenclatural problems of the yeasts should be prepared and submitted to the International Committee on My- c ologic a1 Nome nc latur e .

REFERENCES

Behrend, G. Ueber Trichomycosis nodosd (Juhel-Rdnoy) ; Piedra(0sorio). Berlin, klin. Wochenschr, -27:464- 467 1890. Clements, F. E. and C. L. Shear, The Genera of Fungi second ed. 1931. DeToni, J. B. Saccharomycetaceae. In Saccardo, P. A., Sylloge Fungorum 8: 916. 1889. Derx, H. G. Itersonilia, noveau genre de Sporobolomycktes b myce'lium boucl6. Bull. bot. Gardens, Buitenzorg. ser. 111, 17 (4): 465-72. 1948. LodderTJ. and N. J. W. Kreger-van Rij. The Yeasts. A Taxonomic Review. pp. XI, 713. Amsterdam andNew York. 1952, Reess, Max. Botanische Untersuchungen tiber die Alkohol- gahrungspilze, Leipzig. 187 0. Stelling-Defier, N. M. Die sporogenen Hefen. ErhandeL koninkl. Akad. Wetenschap. af. Naturkunde. Sect. 11. -28' 1931.